Differences among A. thaliana ecotypes in response to infection drives patterns of virus adaptation

Resumen del trabajo presentado al B-Debate: "When Development Meets Stress: Understanding developmental reprogramming upon pathogenesis in plants", celebrado en el CosmoCaixa de Barcelona (España) del 3 al 4 de septiembre de 2018.It is generally assumed that genetic variability in host species for susceptibility to infection will necessarily condition the evolution of viral populations, either by driving them to the diversification of the virus into antigenically diverse strains that track the different host defense alleles, or by canalization of the virus to infect only the most susceptible genotypes. Associated to these processes, virulence may or may not increase concomitantly. In any case, the pathogen’s fitness must be optimized. To tackle these questions, we have been performing evolution experiments with tobacco etch (TEV) and turnip mosaic (TuMV) potyviruses in different genotypes of the experimental host Arabidopsis thaliana. In a first set of experiments, we explored the role of within-host species genetic variability for susceptibility to infection in the extent of TEV local adaptation and virulence. Results were always consistent with a pattern of local adaptation, characterized by a higher infectivity and virulence on the host ecotype(s) encountered during evolution. However, local adaptation not always paid a cost on the foreign host ecotypes: viral lineages evolved in more susceptible ecotypes evolved as specialists, whereas adaptation to the less susceptible ecotypes always resulted in more virulent generalist viruses. Therefore, the antagonistic pleiotropy cost of generalism depends on the characteristics of each particular pathosystem. In a second set of experiments, we are exploring the effect that the amount of genetic diversity for susceptibility has on the rate of TuMV adaptation to different experimental host populations. In good agreement with theoretical expectations, we have found that viral lineages evolving in host populations composed by multiple ecotypes and with maximal genetic diversity evolved slower and were quickly dominated by mild generalist viruses. By contrast, genetically homogeneous host populations composed by a single plant ecotype rapidly selected for locally-adapted more virulent specialists. Finally, in a third set of ongoing experiments, we are evolving TuMV lineages in mutant genotypes of the Col-0 ecotype. Each of these genotypes differ in mutations in genes involved in resistance pathways (e.g., RNAi-mediated, methylationmediated and ethylene and salicylic acid pathways) and in genes whose products have been shown to be essential for TuMV or other potyviruses to complete its infection cycle (e.g., translation initiation factors or heat-shock proteins). Plant genotypes can be classified into three categories according to their response to infection: hypersusceptible, equal to the wildtype and hyposusceptible. TuMV is more infectious and induces severer symptoms in hypersusceptible plant genotypes than those observed in Col-0. By contrast, it is less infectious and induces weaker or no symptoms in hyposusceptible genotypes.Peer reviewe